Marine Crenarchaeota are the most abundant single group of prokaryotes in the ocean, but their physiology and role in marine biogeochemical cycles are unknown. Recently, a member of this clade was isolated from a sea aquarium and shown to be capable of nitrification, tentatively suggesting that Crenarchaeota may play a role in the oceanic nitrogen cycle. We enriched a crenarchaeote from North Sea water and showed that its abundance, and not that of bacteria, correlates with ammonium oxidation to nitrite. A time series study in the North Sea revealed that the abundance of the gene encoding for the archaeal ammonia monooxygenase alfa subunit ( amoA ) is correlated with a decline in ammonium concentrations and with the abundance of Crenarchaeota. Remarkably, the archaeal amoA abundance was 1–2 orders of magnitude higher than those of bacterial nitrifiers, which are commonly thought to mediate the oxidation of ammonium to nitrite in marine environments. Analysis of Atlantic waters of the upper 1,000 m, where most of the ammonium regeneration and oxidation takes place, showed that crenarchaeotal amoA copy numbers are also 1–3 orders of magnitude higher than those of bacterial amoA . Our data thus suggest a major role for Archaea in oceanic nitrification.
Fluorescence in situ hybridization (FISH) in combination with polynucleotide probes revealed that the two major groups of planktonic Archaea (Crenarchaeota and Euryarchaeota) exhibit a different distribution pattern in the water column of the Pacific subtropical gyre and in the Antarctic Circumpolar Current system. While Euryarchaeota were found to be more dominant in nearsurface waters, Crenarchaeota were relatively more abundant in the mesopelagic and bathypelagic waters. We determined the abundance of archaea in the mesopelagic and bathypelagic North Atlantic along a south-north transect of more than 4,000 km. Using an improved catalyzed reporter deposition-FISH (CARD-FISH) method and specific oligonucleotide probes, we found that archaea were consistently more abundant than bacteria below a 100-m depth. Combining microautoradiography with CARD-FISH revealed a high fraction of metabolically active cells in the deep ocean. Even at a 3,000-m depth, about 16% of the bacteria were taking up leucine. The percentage of Euryarchaeota and Crenarchaeaota taking up leucine did not follow a specific trend, with depths ranging from 6 to 35% and 3 to 18%, respectively. The fraction of Crenarchaeota taking up inorganic carbon increased with depth, while Euryarchaeota taking up inorganic carbon decreased from 200 m to 3,000 m in depth. The ability of archaea to take up inorganic carbon was used as a proxy to estimate archaeal cell production and to compare this archaeal production with total prokaryotic production measured via leucine incorporation. We estimate that archaeal production in the mesopelagic and bathypelagic North Atlantic contributes between 13 to 27% to the total prokaryotic production in the oxygen minimum layer and 41 to 84% in the Labrador Sea Water, declining to 10 to 20% in the North Atlantic Deep Water. Thus, planktonic archaea are actively growing in the dark ocean although at lower growth rates than bacteria and might play a significant role in the oceanic carbon cycle.
The recently developed CARD-FISH protocol was refined for the detection of marine Archaea by replacing the lysozyme permeabilization treatment with proteinase K. This modification resulted in about twofold-higher detection rates for Archaea in deep waters. Using this method in combination with microautoradiography, we found that Archaea are more abundant than Bacteria (42% versus 32% of 4,6-diamidino-2-phenylindole counts) in the deep waters of the North Atlantic and that a larger fraction of Archaea than of Bacteria takes up L-aspartic acid (19% versus 10%).
To determine the effects of Saharan dust on the abundance, biomass, community structure, and metabolic activity of oceanic microbial plankton, we conducted eight bioassay experiments between ca. 30uN and 30uS in the central Atlantic Ocean. We found that, although bulk abundance and biomass tended to remain unchanged, different groups of phytoplankton and bacterioplankton responded differently to Saharan dust addition. The predominant type of metabolic response depended on the ecosystem's degree of oligotrophy and was modulated by competition for nutrients between phytoplankton and heterotrophic bacteria. The relative increase in bacterial production, which was the dominant response to dust addition in ultraoligotrophic environments, became larger with increasing oligotrophy. In contrast, primary production, which was stimulated only in the least oligotrophic waters, became less responsive to dust as the ecosystem's degree of oligotrophy increased. Given the divergent consequences of a predominantly bacterial vs. phytoplanktonic response, dust inputs can, depending on the ecosystem's degree of oligotrophy, stimulate or weaken biological CO 2 drawdown. Thus, the biogeochemical implications of changing dust fluxes might not be universal, but variable through both space and time.
We determined the contribution of the three major prokaryotic groups (Bacteria, Crenarchaeota, and Euryarchaeota) on the uptake of D-and L-aspartic acid (Asp) in the major water masses of the North Atlantic (from 100-to 4,000-m depth) with the use of microautoradiography combined with catalyzed reporter deposition fluorescence in situ hybridization (MICRO-CARD-FISH). The percentage of prokaryotic cells that assimilated D-and L-Asp ranged from Ͻ5% to 25%. In the meso-and bathypelagic waters of the North Atlantic, Archaea are more abundant (42% Ϯ 2% of 4Ј,6Ј-diamino-2-phenylindole [DAPI]-stained cells) than Bacteria (30% Ϯ 1% of DAPI-stained cells), and more archaeal than bacterial cells are actively incorporating D-Asp (62% Ϯ 2% vs. 38% Ϯ 2% of total D-Asp active cells). In contrast, Bacteria and Archaea almost equally contribute to L-Asp use in the deep waters of the North Atlantic (47% Ϯ 2% vs. 53% Ϯ 2% of total L-Asp active cells). The increase in the D-Asp : L-Asp uptake ratio in the prokaryotic community with depth appears to be driven by the efficient uptake of D-Asp by, especially, the Crenarchaeota in the deep waters. Because Archaea, and particularly Crenarchaeota, commonly dominate the prokaryotic communities in the ocean's interior, we suggest that they represent a previously unrecognized sink of D-amino acids in the deep ocean.The formation of the North Atlantic Deep Water (NADW) is the major driving force of the oceanic conveyor belt system that, in turn, influences the global climate (Broecker 1997). The turnover time of this oceanic conveyor belt system is about 2,000 yr, whereas that of the dissolved organic carbon (DOC) in the oceanic deep water is about 6,000-8,000 yr (Williams 2000). Hansell and Carlson (1998) showed that the deep water DOC concentrations decline from the deep North Atlantic (ϳ45 mol L Ϫ1 ) to the opposite end of the conveyor belt circulation, the deep Pacific (ϳ37 mol L Ϫ1 ), indicating net removal of DOC. Despite recent advances in the phylogenetic characterization of deep-water prokaryotic communities, little is known about the metabolically active fraction of the prokaryotic community that drives the biogeochemical cycles in the 1 To whom correspondence should be addressed. Present address: Departamento de Ecología y Biología Animal, Universidad de Vigo, 36200, Vigo, Spain (teira@uvigo.es). AcknowledgmentsWe thank the captain and crew of the R/V Pelagia for their help during work at sea.
Dissolved organic carbon (DOC) production by microbial populations was measured at 19 stations in the Atlantic Ocean to quantify the fraction of photoassimilated carbon that flows through the dissolved organic pool at basin scale and to assess the relationship between the percentage of DOC production, phytoplankton size structure, and rates of net community production. Experiments were conducted during four cruises carried out between May 1998 and October 1999, covering three upwelling regions: Benguela (SW Africa), Mauritania (NW Africa) and NW Spain, and the oligotrophic North Atlantic subtropical gyre between 30ЊN and 36ЊN. Photic zone integrated particulate organic carbon (POC) production rates ranged from 10 to 1,178 mg C m Ϫ2 h Ϫ1, thus covering a wide productivity spectrum. The percentage of DOC production with respect to total integrated primary production ranged from 4 to 42%, being larger in oligotrophic, picoplankton-dominated waters, where a balanced metabolism of the microbial community was observed, than in productive, net autotrophic waters, where large-sized cells formed the bulk of the phytoplankton biomass. A highly significant relationship was calculated between DOC and POC production rates in upwelling conditions. By contrast, the relationship between these variables in oligotrophic environments was weak, which suggests that different processes could be controlling the release of dissolved organic matter in productive and unproductive waters.Dissolved organic matter (DOM) is one of the least understood pools of marine matter and represents a major reservoir of organic carbon in the ocean. A large fraction of the dissolved organic carbon (DOC) present in the ocean ultimately derives from primary producers. However, a great deal of controversy still exists on the ecological significance and the ultimate control of DOC production in the ocean.The magnitude of DOC-related fluxes remains still largely uncertain, especially in oligotrophic regions. The high rates of DOC uptake by heterotrophic bacteria in relation to primary production recently measured in unproductive waters (e.g., Hansell et al. 1995;del Giorgio et al. 1997), largely justifies the growing biogeochemical interest of measuring and modeling DOC production in planktonic ecosystems.Initially, the radioactive carbon method for primary production estimation was modified for the measurement of direct excretion of dissolved organic compounds from algal cells. More recently, it has been recognized that several processes, besides direct excretion from intact algal cells, are 1 Corresponding author (eteira@uvigo.es). AcknowledgmentsWe thank G. Tilstone, B. Mouriño, C. Cariño, and C. Robinson for their contributions to the collection of data. Thanks to P. J. le B. Williams for the generous loan of analytical equipment used on the AMT-6 cruise. We are indebted to the captain and crew of research vessels, as well as to all the colleagues on board during the four cruises. We appreciate the comments of two anonymous referees, which improv...
A knowledge of the balance between plankton gross primary production (GPP) and community respiration (CR) in the open ocean is vital to the accurate determination of the global carbon cycle, yet the paucity of open ocean measurements severely limits our understanding. This study measured GPP, net community production, dark CR, and size-fractionated primary production in the upper 200 m of a 12,100 km latitudinal (32ЊS-48ЊN) transect in the Eastern Atlantic Ocean during May and June 1998. This comprehensive data set, which spans five contrasting plankton regimes, including two open ocean oligotrophic provinces, is used to derive a GPP : CR relationship, which suggests that net heterotrophy (GPP Ͻ CR) prevails in the eastern Atlantic when primary production falls below ϳ100 mmol O 2 m Ϫ2 d Ϫ1 . The predictive capability of this relationship is compared with that of the only other published relationship based on similar methodologies and is found to give a more representative description of the autotrophic (GPP Ͼ CR) to heterotrophic seasonal cycle in the Bay of Biscay. This improved predictive power is attributed to the increased representativeness of the current data set. Specifically, the interpretation suggests that the influence of community structure on net ecosystem metabolism implies that prediction of GPP : CR balances in pelagic ecosystems can be best achieved by use of a data set that covers a wide range of community structure and not only a wide range in the magnitude of primary production.
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